Perithecial Ascomycetes from the 400 Million Year Old Rhynie Chert: an Example of Ancestral Polymorphism

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Perithecial Ascomycetes from the 400 Million Year Old Rhynie Chert: an Example of Ancestral Polymorphism Mycologia, 97(1), 2005, pp. 269±285. q 2005 by The Mycological Society of America, Lawrence, KS 66044-8897 Perithecial ascomycetes from the 400 million year old Rhynie chert: an example of ancestral polymorphism Editor's note: Unfortunately, the plates for this article published in the December 2004 issue of Mycologia 96(6):1403±1419 were misprinted. This contribution includes the description of a new genus and a new species. The name of a new taxon of fossil plants must be accompanied by an illustration or ®gure showing the essential characters (ICBN, Art. 38.1). This requirement was not met in the previous printing, and as a result we are publishing the entire paper again to correct the error. We apologize to the authors. T.N. Taylor1 terpreted as the anamorph of the fungus. Conidioge- Department of Ecology and Evolutionary Biology, and nesis is thallic, basipetal and probably of the holoar- Natural History Museum and Biodiversity Research thric-type; arthrospores are cube-shaped. Some peri- Center, University of Kansas, Lawrence, Kansas thecia contain mycoparasites in the form of hyphae 66045 and thick-walled spores of various sizes. The structure H. Hass and morphology of the fossil fungus is compared H. Kerp with modern ascomycetes that produce perithecial as- Forschungsstelle fuÈr PalaÈobotanik, Westfalische cocarps, and characters that de®ne the fungus are Wilhelms-UniversitaÈt MuÈnster, Germany considered in the context of ascomycete phylogeny. M. Krings Key words: anamorph, arthrospores, ascomycete, Bayerische Staatssammlung fuÈr PalaÈontologie und ascospores, conidia, fossil fungi, Lower Devonian, my- Geologie, Richard-Wagner-Straûe 10, 80333 MuÈnchen, coparasite, perithecium, Rhynie chert, teleomorph Germany R.T. Hanlin Department of Plant Pathology, University of Georgia, INTRODUCTION Athens, Georgia 30602 Among the true fungi the Ascomycota is the largest group, containing more than 3000 genera and ap- Abstract: We describe a perithecial, pleomorphic as- proximately 32 000 species, and includes a variety of comycetous fungus from the Early Devonian (400 associations with plants, animals, green algae and cy- mya) Rhynie chert; the fungus occurs in the cortex anobacteria. The principal morphological feature just beneath the epidermis of aerial stems and rhi- that distinguishes ascomycetes from other fungi is the zomes of the vascular plant Asteroxylon. Perithecia are sac-like structure termed the ascus in which the sex- nearly spherical with a short, ostiolate neck that ex- ual ascospores are produced. Although historically tends into a substomatal chamber of the host plant; there have been several major classi®cations of asco- periphyses line the inner surface of the ostiole. The mycetes (Hawksworth et al 1995), the recent use of ascocarp wall is multilayered and formed of septate gene sequence data has resulted in the recognition hyphae; extending from the inner surface are elon- of three major groups (e.g. Liu et al 1999). These gate asci interspersed with delicate paraphyses. Asci include the Archiascomycetes, or the unicellular appear to be unitunicate and contain up to 16 yeast-like forms, the Ascomycetous yeasts or Sacchar- smooth, uniseriate-biseriate ascospores. The method omycetales and the Euascomycetes or ®lamentous of ascospore liberation is unknown; however, the tip forms that enclose their asci in or on an ascoma (Al- of the ascus is characterized by a narrow, slightly el- exopoulos et al 1996). Among this latter group, the evated circular collar. Ascospores appear 1±5 celled, discomycetes, loculoascomycetes, pyrenomycetes and and germination is from one end of the spore. Also plectomycetes form a well-supported monophyletic present along the stems and interspersed among the group (Berbee and Taylor 2001). The pyrenomycetes perithecia are acervuli of conidiophores that are in- and plectomycetes historically are distinguished based on features of the ascoma (Barr 2001). Plec- Accepted for publication April 27, 2004. tomycetes include fungi with nonostiolate cleistothe- 1 Corresponding author. E-mail: [email protected] cia that contain multiple layers of asci, and asco- 269 270 MYCOLOGIA spores are typically unicellular. The pyrenomycetes parsimonious trees were obtained, each 12 steps long. The are characterized generally by ¯ask-shaped, ostiolate analysis did not include anamorphic features. perithecia that produce ovoid to cylindrical persistent asci. Asci are produced in a hymenium that also may TAXONOMY contain sterile hyphae. Ascospores often are dis- charged forcibly and may be one to several celled. Paleopyrenomycites Taylor, Hass, Kerp, Krings et As a result of a renewed interest in the Lower De- Hanlin gen. nov. vonian Rhynie chert, numerous fungi have been Generic diagnosis. Ascocarp of globose, nearly identi®ed that include several members of the Chy- spherical perithecia with short neck positioned be- tridiomycetes (Taylor et al 1992b), including a blas- neath host stoma; perithecium wall of two layers of tocladialean (Remy et al 1994a). Also present are sev- septate hyphae; ostiole lined with periphyses, hyme- eral examples of mycoparasites (Hass et al 1994), par- nium of elongate, unitunicate asci and paraphyses, asites (Taylor et al 1992a), a glomeromycete includ- ascospores uni- to perhaps multicelled, elongate with ing the formation of endomycorrhizae in the land monopolar germination; conidiophores unbranched plant Aglaophyton (Remy et al 1994b, Taylor et al as acervuli; conidiogenesis thallic, basipetal, and pos- 1995), and a lichen formed by a cyanobacterium and sibly holoarthric; arthrospores cube-shaped. a fungus (Taylor et al 1997). Well preserved fungal remains within the Rhynie chert can be identi®ed as pyrenomycetes that contain asci and ascospores (Tay- P. devonicus Taylor, Hass, Kerp, Krings et Hanlin lor et al 1999). Also present on the same host are Speci®c diagnosis. Perithecia beneath epidermis in m conidiophores. These teleomorphic and anamorphic outer cortical tissues of host, up to 400 m diam with m forms, together with various stages in the develop- short (50 m) neck; perithecium wall multilayered m ment of the fungus, provide the opportunity to char- with an inner zone of large (5±9 m), irregularly ori- ented hyphae and outer, slightly thicker zone of small acterize a new fossil in the Early Devonian ecosystem m that can be compared with certain modern ®lamen- (3±5 m), shorter hyphae that tend to parallel sur- tous ascomycetes. It is the intent of this paper to de- face of perithecium wall; hymenium extending to just scribe a perithecial ascomycete from the Rhynie chert below level of ostiole and formed of intermixed elon- gate asci and paraphyses, asci nonsynchronous in de- containing exceptionally well preserved asci and as- m m cospores (Taylor et al 1999), in addition to the ana- velopment, 40±50 m long and 10±15 m wide, cla- morphic state of the fungus. vate with a narrow base, ascus tip operculate with a narrow collar; paraphyses thin-walled and extending upward from inner wall to a level slightly above asci; MATERIALS AND METHODS up to 16 ascospores per ascus in both uniseriate and biseriate arrangement, ascospores unornamented, The Rhynie chert site consists of more than 10 plant-bear- smooth, up to 10 mm long, 1±5 (?) celled, germina- ing beds that are represented as siliceous sinters (Trewin tion at narrow end forming narrow unbranched hy- and Rice 1992). Information on the geology and setting of pha; conidiophores up to 600 mm long and 10 mm Rhynie chert can be found in Rice et al (2002). The age of 3 m the chert generally is considered to be Pragian (Early De- diam, septate, arthrospores 4 5 m diam. vonian) based on palynomorph assemblages (Richardson Holotype. Specimen in petrographic thin section 1967) and radiometric dating (Rice et al 1995). The peri- slide PB 3411 in the W. Remy Collection permanently thecia occur in the cortex of the land plant Asteroxylon deposited in the Forschungsstelle fuÈr PalaÈobotanik, mackiei and were studied by means of petrographic thin WestfaÈlische Wilhelms-UniversitaÈt, MuÈnster; FIGS.2, sections prepared by cementing a small piece of the chert 7, 12, 22±24 in this paper. containing the fungus to a microscope slide and grinding Paratypes. Perithecia present in slides PB3401, the chert to a thickness of approximately 50±150 mm. Ob- 3404, 3409, 3410, 3412, 3413, 3414, 3416, 3417, 3418, servations and micrographs were prepared using oil im- 3433, 3436, 3437, 3441, 3445, 3469 in the above col- mersion objectives directly on the polished rock surface lection; FIGS. 1, 3±6, 8±11, 13±21, 25±45 in this paper. without cover glasses. Slides are deposited in the Paleobo- Type locality. Rhynie, Aberdeenshire, Scotland. Na- tanical Collection in the Forschungsstelle fuÈr PalaÈobotanik, tional Grid Reference NJ 494276 (Edwards 1986). WestfaÈlische Wilhelms-UniversitaÈt, MuÈnster, Germany. Ac- quisition numbers and types are noted in the ®gure descrip- Age. Early Devonian. tions and in the diagnosis. Stratigraphic position. Pragian. Twelve morphological characters from Barr (2001) for Etymology. The generic name is Paleopyrenomycites nine ascomycete taxa and Paleopyrenomycites were analyzed is proposed as a combination of palaios, ancient, and under maximum parsimony using PAUP 4.0. The analysis the informal class of ascomycetes, pyrenomycetes; the was performed using exhaustive search. A total of 64 most ending ites is used to designate a fossil taxon as sug- TAYLOR ET AL:FOSSIL ASCOMYCETES 271 FIGS. 1±6. Paleopyrenomycites devonicus. 1. Transverse section of Asteroxylon rhizome with numerous perithecia (arrows) in cortex just beneath epidermis. Slide 3404, Bar 5 1.0 mm. 2. Older aerial stem at transition level with cortical trabeculae (arrow). Perithecium (P) the same as that in FIG. 7. Slide 3411, Bar 5 1.0 mm. 3. Several closely associated perithecia. Note necrotic area (arrow) in cortex. Slide 3409, Bar 5 0.5 mm. 4. Partially decayed stem showing three perithecia; wall of perithecium disassociated (arrow). Slide 3433, Bar 5 250 mm. 5. Cluster of mature perithecia (P) in cortex. Note oblique section of perithecium just beneath thickened guard cells and stoma (S).
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